Organization of the sleep-related neural systems in the brain of the harbour porpoise (Phocoena phocoena)

• Published in: Journal of comparative neurology (1911) 2016-07, Vol.524 (10), p.1999-2017
• Main Authors: Dell, Leigh-Anne, Patzke, Nina, Spocter, Muhammad A., Siegel, Jerome M., Manger, Paul R.
• Format: Article
• Language: English
• Subjects: Animals; Brain - cytology; Brain - physiology; brain evolution; Brain Mapping; Calbindin 2 - metabolism; Calbindins - metabolism; Cetacea; Cetartiodactyla; Choline O-Acetyltransferase - metabolism; Male; mammalian sleep; Nerve Net - metabolism; Neurons - metabolism; Odontocete; Odontoceti; Parvalbumins - metabolism; Phocoena - anatomy & histology; Phocoena - physiology; Phocoena phocoena; RRID AB_10000321; RRID AB_10000323; RRID AB_10000340; RRID AB_10000343; RRID AB_2079751; Serotonin - metabolism; Sleep - physiology; Tyrosine 3-Monooxygenase - metabolism; unihemispheric sleep
• ISSN: 0021-9967; 1096-9861
• DOI: 10.1002/cne.23929

ABSTRACT The present study provides the first systematic immunohistochemical neuroanatomical investigation of the systems involved in the control and regulation of sleep in an odontocete cetacean, the harbor porpoise (Phocoena phocoena). The odontocete cetaceans show an unusual form of mammalian sleep, with unihemispheric slow waves, suppressed REM sleep, and continuous bodily movement. All the neural elements involved in sleep regulation and control found in bihemispheric sleeping mammals were present in the harbor porpoise, with no specific nuclei being absent, and no novel nuclei being present. This qualitative similarity of nuclear organization relates to the cholinergic, noradrenergic, serotonergic, and orexinergic systems and is extended to the γ‐aminobutyric acid (GABA)ergic elements involved with these nuclei. Quantitative analysis of the cholinergic and noradrenergic nuclei of the pontine region revealed that in comparison with other mammals, the numbers of pontine cholinergic (126,776) and noradrenergic (122,878) neurons are markedly higher than in other large‐brained bihemispheric sleeping mammals. The diminutive telencephalic commissures (anterior commissure, corpus callosum, and hippocampal commissure) along with an enlarged posterior commissure and supernumerary pontine cholinergic and noradrenergic neurons indicate that the control of unihemispheric slow‐wave sleep is likely to be a function of interpontine competition, facilitated through the posterior commissure, in response to unilateral telencephalic input related to the drive for sleep. In addition, an expanded peripheral division of the dorsal raphe nuclear complex appears likely to play a role in the suppression of REM sleep in odontocete cetaceans. Thus, the current study provides several clues to the understanding of the neural control of the unusual sleep phenomenology present in odontocete cetaceans. J. Comp. Neurol. 524:1999–2017, 2016. © 2016 Wiley Periodicals, Inc. Using immunohistochemical methods, we examined the sleep–wake neural systems in the brain of the harbor porpoise. We found that quantitative, rather than qualitative, differences in the pontine nuclei, such as the locus coeruleus, appear to allow cetaceans to sleep with half their brain at a time.